Abstract
Flavonoids have a variety of biological functions including UV protectant, antioxidant, allelopathy and auxin transport inhibitor in plants. In addition, flavonoids are implicated in defense response against pathogens. In this study, we found that kaempferol, a kind of flavonol, induces bacterial pathogen resistance. In addition, we identified the signaling pathway to explain how kaempferol can induce pathogen resistance in Arabidopsis. We showed that kaempferol upregulates the transcription of two pathogenesis-related (PR) genes. Interestingly, the monomerization and nuclear translocation of NPR1, a key regulator of PR gene expression, was induced by kaempferol through the accumulation of salicylic acid (SA). Furthermore, we found that the kaempferol-induced monomerization of NPR1 is mediated by the activation of MPK3 and MPK6. Taken together, this study suggests that kaempferol induces pathogen resistance by both SA and MPK-dependent signaling pathways in Arabidopsis.
Similar content being viewed by others
Data availability
The datasets generated and/or analysed during the current study are available from the corresponding author on reasonable request.
References
An J, Kim SH, Bahk S, Vuong UT, Nguyen NT, Do HL, Kim SH, Chung WS (2021) Naringenin induces pathogen resistance against pseudomonas syringae through the activation of NPR1 in Arabidopsis. Front Plant Sci 12:672552
Backer R, Naidoo S, van den Berg N (2019) The nonexpressor of pathogenesis-related genes 1 (NPR1) and related family: mechanistic insights in plant disease resistance. Front Plant Sci 10:102
Brunetti C, Di Ferdinando M, Fini A, Pollastri S, Tattini M (2013) Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans. Int J Mol Sci 14:3540–3555
Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52:98–111
Chai J, Liu J, Zhou J, Xing D (2014) Mitogen-activated protein kinase 6 regulates NPR1 gene expression and activation during leaf senescence induced by salicylic acid. J Exp Bot 65:6513–6528
Ding P, Ding Y (2020) Stories of salicylic acid: a plant defense hormone. Trends Plant Sci 25:549–565
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Eghbaliferiz S, Iranshahi M (2016) Prooxidant activity of polyphenols, flavonoids, anthocyanins and carotenoids: updated review of mechanisms and catalyzing metals. Phyther Res 30:1379–1391
Falcone Ferreyra ML, Rius SP, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3:222
Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N et al (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–232
Gassmann W (2005) Natural variation in the Arabidopsis response to the avirulence gene hopPsyA uncouples the hypersensitive response from disease resistance. Mol Plant-Microbe Interact 18:1054–1060
Jagodzik P, Tajdel-Zielinska M, Ciesla A, Marczak M, Ludwikow A (2018) Mitogen-activated protein kinase cascades in plant hormone signaling. Front Plant Sci 9:1–26
Jia Z, Zou B, Wang X, Qiu J, Ma H, Gou Z, Song S, Dong H (2010) Quercetin-induced H2O2 mediates the pathogen resistance against Pseudomonas syringae pv. tomato DC3000 in Arabidopsis thaliana. Biochem Biophys Res Commun 396:522–527
Kim HS, Delaney TP (2002) Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J 32:151–163
Kim SH, Kim HS, Bahk S, An J, Yoo Y, Kim JY, Chung WS (2017) Phosphorylation of the transcriptional repressor MYB15 by mitogen-activated protein kinase 6 is required for freezing tolerance in Arabidopsis. Nucleic Acids Res 45:6613–6627
Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339–2350
Kuhn BM, Geisler M, Bigler L, Ringli C (2011) Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol 156:585–595
Maier F, Zwicker S, Huckelhoven A, Meissner M, Funk J, Pfitzner AJP, Pfitzner UM (2011) Nonexpressor of pathogenesis-related proteins1 (NPR1) and some NPR1-related proteins are sensitive to salicylic acid. Mol Plant Pathol 12:73–91
Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266
Mierziak J, Kostyn K, Kulma A (2014) Flavonoids as important molecules of plant interactions with the environment. Molecules 19:16240–16265
Mol J, Grotewold E, Koes R (1998) How genes paint flowers and seeds. Trends Plant Sci 3:212–217
Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 80(312):436–439
Nguyen NT, Kim SH, Kim KE, Bahk S, Nguyen XC, Kim MG, Hong JC, Chung WS (2022) Ca2+/CaM increases the necrotrophic pathogen resistance through the inhibition of a CaM-regulated dual-specificity protein phosphatase 1 in Arabidopsis. Plant Biotechnol Rep 16:71–78
Nie S, Xu H (2016) Riboflavin-induced disease resistance requires the mitogen-activated protein kinases 3 and 6 in Arabidopsis thaliana. PLoS One 11:e0153175
Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography–mass spectrometry. Nat Protoc 5:986–992
Panche AN, Diwan AD, Chandra SR (2016) Flavonoids: an overview. J Nutr Sci 5:e47
Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563
Procházková D, Boušová I, Wilhelmová N (2011) Antioxidant and prooxidant properties of flavonoids. Fitoterapia 82:513–523
Qi Q, Guo Z, Liang Y, Li K, Xu H (2019) Hydrogen sulfide alleviates oxidative damage under excess nitrate stress through MAPK/NO signaling in cucumber. Plant Physiol Biochem 135:1–8
Rice-Evans C (2001) Flavonoid antioxidants. Curr Med Chem 8:797–807
Rice-Evans CA, Miller NJ, Paganga G (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20:933–956
Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343
Shine MB, Yang JW, El-Habbak M, Nagyabhyru P, Fu DQ, Navarre D, Ghabrial S, Kachroo P, Kachroo A (2016) Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. New Phytol 212:627–636
Shirley BW (1996) Flavonoid biosynthesis: ‘new’ functions for an ‘old’ pathway. Trends Plant Sci 1:377–382
Sun T, Zhang Y, Li Y, Zhang Q, Ding Y, Zhang Y (2015) ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nat Commun 6:10159
Takahashi A, Ohnishi T (2004) The significance of the study about the biological effects of solar ultraviolet radiation using the exposed facility on the international space station. Biol Sci Sp 18:255–260
Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323
Thulasi Devendrakumar K, Li X, Zhang Y (2018) MAP kinase signalling: interplays between plant PAMP- and effector-triggered immunity. Cell Mol Life Sci 75:2981–2989
Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403
Tsuda K, Katagiri F (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol 13:459–465
Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Network properties of robust immunity in plants. PLoS Genet 5:e1000772
Vandeputte OM, Kiendrebeogo M, Rasamiravaka T, Stévigny C, Duez P, Rajaonson S, Diallo B, Mol A, Baucher M, el Jaziri M (2011) The flavanone naringenin reduces the production of quorum sensing-controlled virulence factors in pseudomonas aeruginosa PAO1. Microbiology 157:2120–2132
Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790
Wang Y, Schuck S, Wu J, Yang P, Döring A-C, Zeier J, Tsuda K (2018) A MPK3/6-WRKY33-ALD1-pipecolic acid regulatory loop contributes to systemic acquired resistance. Plant Cell 30:2480–2494
Wing-Cheung Leung H, Kuo CL, Yang WH, Lin CH, Lee HZ (2006) Antioxidant enzymes activity involvement in luteolin-induced human lung squamous carcinoma CH27 cell apoptosis. Eur J Pharmacol 534:12–18
Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647
Yang W, Xu X, Li Y, Wang Y, Li M, Wang Y, Ding X, Chu Z (2016) Rutin-mediated priming of plant resistance to three bacterial pathogens initiating the early SA signal pathway. PLoS One 11:e0146910
Yedidia I, Schultz K, Golan A, Gottlieb HE, Kerem Z (2019) Structural elucidation of three novel kaempferol O-tri-glycosides that are involved in the defense response of hybrid ornithogalum to pectobacterium carotovorum. Molecules 24:2910
Zhang Y, Li X (2019) Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol 50:29–36
Zhang M, Su J, Zhang Y, Xu J, Zhang S (2018) Conveying endogenous and exogenous signals: MAPK cascades in plant growth and defense. Curr Opin Plant Biol 45:1–10
Zhou J, Wang X, He Y, Sang T, Wang P, Dai S, Zhang S, Meng X (2020) Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. Plant Cell 32:2621–2638
Acknowledgements
This research was supported by a grant from the Cooperative Research Program for Agriculture Science and Technology Development (No. PJ01590901) funded by the Rural Development Administration, Republic of Korea and by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (No. 2021R1A6A3A01088557) and partly supported by the Vietnam National Foundation for Science and Technology Development (NAFOSTED) (No. 106.02-2017.09) and by the National Institute of Ecology (NIE-B-2022-15).
Author information
Authors and Affiliations
Contributions
JA, XCN, HCP and WSC designed, planned and organized the experiments. JA, HK, MLAP, ZR and JP performed the experiments. JA, XCN, SB, SHK and SHK analyzed the data. JA, XCN, SHK, HCP and WSC wrote the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
An, J., Nguyen, X.C., Kim, S.H. et al. Kaempferol promotes bacterial pathogen resistance through the activation of NPR1 by both SA and MPK signaling pathways in Arabidopsis. Plant Biotechnol Rep 16, 655–663 (2022). https://doi.org/10.1007/s11816-022-00806-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11816-022-00806-5